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Fruit Decay to Diseases: Can Induced Resistanceand Priming Help?Petriacq, Pierre; Lopez, Ana; Luna Diez, Estrella

DOI:10.3390/plants7040077

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Citation for published version (Harvard):Petriacq, P, Lopez, A & Luna Diez, E 2018, 'Fruit Decay to Diseases: Can Induced Resistance and PrimingHelp?', Plants, vol. 7, no. 4, 77. https://doi.org/10.3390/plants7040077

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Fruit Decay to Diseases: Can Induced Resistance and Priming Help?Plants 2018, 7(4), 77; https://doi.org/10.3390/plants7040077

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plants

Review

Fruit Decay to Diseases: Can Induced Resistance andPriming Help?

Pierre Pétriacq 1,2,* , Ana López 3 and Estrella Luna 4,*1 UMR 1332 Biologie du Fruit et Pathologie, Université de Bordeaux et INRA de Bordeaux,

F-33883 Villenave d’Ornon, France2 Plateforme Métabolome Bordeaux-MetaboHUB, Centre de Génomique Fonctionnelle Bordeaux, IBVM,

Centre INRA Bordeaux, F-33140 Villenave d’Ornon, France3 Department of Plant Molecular Genetics, Spanish National Centre for Biotechnology, 28049 Madrid, Spain;

ana.lopez@cnb.csic.es4 School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK* Correspondence: pierre.petriacq@inra.fr (P.P.); e.lunadiez@bham.ac.uk (E.L.);

Tel.: +33-(0)5-57-12-25-75 (P.P.); +44-(0)-121-414-8699 (E.L.)

Received: 29 August 2018; Accepted: 20 September 2018; Published: 21 September 2018�����������������

Abstract: Humanity faces the challenge of having to increase food production to feed an exponentiallygrowing world population, while crop diseases reduce yields to levels that we can no longer afford.Besides, a significant amount of waste is produced after fruit harvest. Fruit decay due to diseases at apost-harvest level can claim up to 50% of the total production worldwide. Currently, the most effectivemeans of disease control is the use of pesticides. However, their use post-harvest is extremely limiteddue to toxicity. The last few decades have witnessed the development of safer methods of diseasecontrol post-harvest. They have all been included in programs with the aim of achieving integratedpest (and disease) management (IPM) to reduce pesticide use to a minimum. Unfortunately, theseapproaches have failed to provide robust solutions. Therefore, it is necessary to develop alternativestrategies that would result in effective control. Exploiting the immune capacity of plants has beendescribed as a plausible route to prevent diseases post-harvest. Post-harvest-induced resistance (IR)through the use of safer chemicals from biological origin, biocontrol, and physical means has alsobeen reported. In this review, we summarize the successful activity of these different strategies andexplore the mechanisms behind. We further explore the concept of priming, and how its long-lastingand broad-spectrum nature could contribute to fruit resistance.

Keywords: fruit decay; integrated pest management (IPM); post-harvest diseases; inducedresistance; priming

1. Background

Fruit and vegetables represent a major source of food worldwide. They contain a battery of naturalcompounds with various health benefits, including vitamins, proteins, fibres and minerals. As such,their consumption is highly recommended globally. Quite strikingly, however, more than a third of fruitand vegetables fails to reach the customer due to infections with pathogenic microbes (e.g., bacteria,fungi, viruses) [1]. This leads to massive losses, both economic and social [1]. Diseases caused bysuch infections are likely to appear in the field (i.e., pre-harvest), but also appear or affect the fruitpost-harvest. Post-harvest losses can dramatically impact fruit production and quality [2], resulting inlosses of an average of 22.5% of the yield in developing countries [3].

However, we live in a world that can no longer afford such high percentages in food wastebecause, due to an increasing growing population, yields need to rise in order to meet food demands [3].

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Importantly, this cannot be done at any cost and should be accomplished in a sustainable manner [3,4].Currently, the most effective methods of control rely on breeding for resistance and the use of chemicalpesticides; however, both strategies are easily overcome by plant pathogens thanks to the evolutionagainst single resistance genes and to chemical targets, respectively [5]. Moreover, the use of chemicalpesticides claims further attention due to their potential toxicity to humans and the environment.This is resulting in a growing social demand, forcing the action of public entities for safe and functionalfood that exploits alternative methods of disease control which could first be used to limit, and thento stop, the use of pesticides [5,6]. In the last few decades, the agri-tech system has put great effortinto developing alternatives that could be framed into the so-called integrated pest (and disease)management (IPM) approach.

Among the different control strategies, many research groups are highlighting the potential thatexploiting the plant immune system can have in disease protection. Plants benefit from their highlyrobust and efficient immune system, allowing them to overcome many biological threats. This isdue to the fact that, apart from their innate strategies, plants have inducible defence mechanisms torespond effectively against specific threats. Moreover, plants have evolved the capacity to sensitizetheir immune system for a better expression of induced defence mechanisms [7]. This phenomenonis known as priming of defence and is understood as an adaptive part of induced resistance (IR) [8].Priming can be first established after stimuli that can have an environmental, biological or chemicalorigin. After perception, plants maintain a “priming phase” where molecular and biochemical changesoccur but where there is not a direct activation of defence mechanisms [9]. Therefore, primingdoes not result in many costs in terms of plant development [8]. The priming phase has beenshown to be long-lasting [10,11] and even to be transmitted to the following generations [12–14].That is, plants exposed to stress stimuli produce progeny that display sensitized defence mechanisms.Upon subsequent attack, priming allows for a faster and stronger activation of defence that ultimatelyresults in broad spectrum disease protection [7]. Therefore, there are many benefits in investigatinghow plants manage priming: (i) it offers an effective defence strategy against many plant pathogensthat are difficult to control by single resistance genes or chemical pesticides [15]; (ii) it results inconsiderable lower costs in plant growth and yield than direct activation of defence responses [16];(iii) it has been documented in many plant and crop species [8]; (iv) the expression of the plant’s owndefence mechanisms is considered a safer and environmentally friendly approach; and (v) the factthat it is maintained through the life of the plant, including fruit stage [17], opens up possibilities fordisease control, both pre- and post-harvest.

In this review, we examine the current knowledge on induced resistance and priming for fruitdefence. We highlight the current major threads and methods of control, explore the knowledge infruit-induced resistance and priming, and examine key aspects of these phenomena that could becombined with current agricultural trends into novel strategies for fruit disease resistance [18].

2. Major Post-Harvest Threats to Agricultural Markets

Fruit are threatened by different microorganisms, such as fungi, bacteria and to a lesser extendviruses, which are the agents of different diseases (Table 1).

Post-harvest, the biggest challenge that the agri-tech market faces is definitely of fungal nature.Fungi, without effective control methods, can result in a loss potential of 24% [1]. Most losses of fruitdiseases of commercial importance result from pre- or post-harvest infections with fungal pathogens.This is because of their highly adaptive lifestyle that allows them to grow and develop under storageconditions. Major fungal threats post-harvest are moulds, mildews and rots that have the capacity toinfect a wide range of plant species.

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Table 1. Examples of major threats for fruit and the main affected crops.

Pathogenic Microbes Threats Crops

Fungi Botrytis cinerea Tomatoes, citrus fruit, grapes, strawberriesPenicillium expansum Apples, citrus fruitPenicillium digitatum Apples, citrus fruitPenicillium italicum Citrus fruitPlasmopara viticola GrapesRhizopus stolonifera StrawberriesAlternaria alternata Tomatoes, grapes

Fusarium spp. MelonsTrichothecium roseum Cucurbits (e.g., melon)

Colletotrichum gloeosporioides Citrus fruit, bananas, mangoes, papayasColletotrichum acutatum Loquats

Guignardia citricarpa Citrus fruitBacteria Clavibacter michiganensis Tomatoes

Xanthomonas axonopodis Tomatoes, peppersSalmonella enterica Tomatoes, melons

Escherichi coli Tomatoes, strawberriesViruses Ringspot virus Papayas

Botrytis cinerea is a necrotrophic fungal pathogen that grows particularly aggressively on thetissues of more than 200 plant species, including fruits and vegetables. B. cinerea is the pathogenic agentresponsible for grey mould and this disease is capable of affecting many crops at a post-harvest level.Plants belonging to the Solanaceae family such as tomato, and other species of agronomical importancesuch as strawberries, red fruit (e.g., raspberries), and citrus fruit, are the most affected by this pathogen.Due to this wide range of hosts, and based on economic and scientific importance, B. cinerea rankedsecond into the world top 10 fungal plant pathogens, and is alone responsible for enormous economiclosses [19]. Another example of a devastating fungal disease post-harvest is Penicillium rots, suchas Penicillium expansum, P. digitatum and P. italicum. Similarly to B. cinerea, Penicillium species causepost-harvest fruit decay in considerable proportions, with P. digitatum being responsible for 90% ofall the citrus fruit waste post-harvest. Whereas P. digitatum and P. italicum are responsible for greenmould (or green rot) in citrus fruit, P. expansum causes blue mould which significantly affects orchardfruit, particularly apples. P. expansum is a wound pathogen that uses brushes, punctures or rubs topenetrate in the fruit tissue [20] and spores can live in the soil and organic material (including deadwood). An important difference with B. cinerea is that with P. expansum serious damage is targetedexclusively at a post-harvest stage. P. expansum can be found in vegetative tissue of trees such as citrusand orchards, however, it rarely produces damage that affects fruit production. Nevertheless, as it canbe present in the fruit upon collection, methods of control that start before the fruit is harvested arenecessary to reduce post-harvest decay to this pathogen. Very importantly, apart from its negativeeffect in fruit decay, P. expansum produces the mycotoxin patulin, a neurotoxic compound that can reachthe markets normally in apples and apple products [21]. In addition to these two major mould diseases,mildews such as Plasmopara viticola and Erysiphe necator, and rots such as Alternaria alternata, also resultin considerable post-harvest decay of grapes and tomatoes, respectively. Finally, Colletotrichum genusfungi trigger anthracnose disease, which is of high importance in many plant species such as bananas,mangoes, papaya and pome fruit.

In addition to fungi, also bacterial pathogens are responsible for post-harvest fruit decay (Table 1).A vast and diverse community of bacteria can be found on the surface of flesh fruits and vegetables [22].For example, infections with Clavibacter michiganensis subsp. sepedonicus cause ring rot in potato andthe subsp. michiganensis the bacterial wilt and canker of tomato [23], causing important economic costsin certain countries and varieties. It is extremely difficult to control due to bacteria surviving for longperiods of time (years) on equipment, storage trays, tools, and other inert surfaces [24]. Other diseases,such as bacterial spot in tomatoes and peppers, are caused by Xanthomonas axonopodis and can alsoresult in serious damage to fruit [25]. However, bacterial pathogens seem to have less impact inpost-harvest fruit decay in comparison to fungal diseases. For instance, there are crops, such as citrus

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fruit, that do not develop bacterial post-harvest disease of commercial importance [26]. Nevertheless,it is very important to consider that, apart from their potential effect on fruit decay, fruit can also hostbacterial human pathogens, thus representing a serious biosecurity cause of concern. Bacteria suchas Salmonella enterica and Escherichia coli are responsible for human infections. Problems with thesebacteria commonly occur in countries where biosecurity and hygienic measures are underdeveloped.However, S. enterica infections in tomato occur because of the bacteria accumulating in the fruit aftertravelling from the rhizosphere. This internal migration is an obscure infection method that is verydifficult to control with conventional and hygienic measures. It was only a few years ago when inGermany, an E. coli outbreak from infected fenugreek sprouts caused serious damage to human healthand the death of at least 55 people [27]. Thus, bacteria of a human pathogenic nature impose a risk in apost-harvest agricultural setting. Currently, there are limited strategies to effectively control them and,therefore, more research is required to limit growth by these strains.

Viruses can also trigger post-harvest fruit decay in different crops, although in comparison tofungal and bacterial diseases, they occur to a much lower extent (Table 1). Typical damage occursduring the growing period in vegetative tissue, thus compromising fruit development and yield ratherthan affecting the fruit directly. Nevertheless, one problematic virus that results in economic lossespost-harvest is the papaya ringspot virus, that affects papaya farming in different countries [28].

There are many threats that challenge production at a post-harvest level. Some of these pathogens,even when causing their biggest damage after fruit harvesting, are known to be already present in theplants during cultivation. Therefore, the implementation of control strategies that target both pre- andpost-harvest levels will have the potential to successfully control diseases that claim yield percentagesthat are not affordable in a world with an ever-increasing population.

3. Current Knowledge of Disease Protection

For decades, there have been many methods developed for the control of post-harvest diseases [5].The use of pesticides [2], biocontrol through antagonistic microbes such as yeast and bacteria [2],the conservation of the microbiome [29], non-toxic agents of plant and other biological origin [30],physical means including ultraviolet (UV) light [31], light-emitting diode (LED) blue light [32],temperature [33], pressure [34], genetic means [35], and the exploitation of the fruit’s own defencecapacity [2], have been thoroughly investigated. The development of all these control methods hasunfortunately not solved the problem of post-harvest waste to diseases due to the outstanding abilityof pathogenic microorganisms to adapt. Pesticide control is arguably the most effective method ofcontrol to date. However, pathogens can easily evolve resistance to the active compounds and dueto their toxicity to humans and the environment, its use is strictly limited and legislated. Under thedirective 2009/128/EC of the European Commission, the use of pesticides at a post-harvest level ishighly restricted by maximun residue limits (MRLs), a factor that specifies the safe maximum amountof pesticide that can be found in a particular product. MRLs guide agricultural systems, agri-techcompanies and other communities in the design and application of products [6]. This legislation ishighly dynamic which makes it complicated to keep up with new requirements. As a consequence,at the moment, there are not many pesticides that can be used at a post-harvest stage. One of themis Imazalil, a product used to prevent fungal pathogens such as P. digitatum in citrus and cucurbitfruit [36]. Even if Imazalil is considered safe at present, its use in post-harvest applications is likelyto be stopped due to the continued reduction in MRLs permitted. Importantly, there are also somecrops, such as tomato and strawberry, where no pesticides can be used to control diseases post-harvest.The agricultural system is therefore trending towards the application of pesticides at earlier statespre-harvest. Pre-harvest treatments when pathogen is still not fully established involves the applicationof a lower amount of the chemical for the same effectiveness, which in turn reduces chemical residuesto comply ultimately with MRLs.

There are several clear advantages of working before the products have been collected: (i) thereis a reduction in the mechanical damage that fruit suffer due to manipulation; (ii) it prevents

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cross-contamination with other diseases during post-harvest treatments; and crucially (iii) it allowsfor an early intervention when the disease is either still not present in the fruit, or is at the earlystages of development. The different pre-harvest strategies are integrated into a battery of measuresto ultimately prevent diseases through IPM. This approach consequently provides benefits at bothharvest levels and aims to reduce the reliance of crops in pesticide control.

This strategy is not only limited to fungicides, and other approaches are being developed atan earlier stage of cultivation to further prevent post-harvest diseases [37]. For example, otherchemicals from plant and other biological origins have proven helpful when applied at a pre-harveststage [38,39]. Hygienic treatments such as heat and chemical disinfection are regularly followed tocombat diseases [40]. They have proven effective in securing that fruit reach storage and distribution inthe cleanest possible conditions. Similarly, disease monitoring pre-harvest represents another strategythat provides guidance for specific treatments later on during post-harvest [41]. In addition, the useof biocontrol is a robust and effective method that serves to protect both the plant during growthand the fruit post-harvest [42]. The long-lasting protection is the result of biocontrol cultures beingmaintained in plants for weeks after inoculation [43], and of the biocontrol initiating its activity atearly stages of infection. The long-lasting effectiveness is, however, more complex to deliver underfield conditions than in controlled environments. Moreover, post-harvest storage conditions can alsoimpact its performance [44].

Overall, even when the market strongly relies on the use of pesticides, this approach is highlylimited and new methods of control have been developed. The novel strategies, however, may lack theexpected and needed effectiveness in controlling fruit decay and, therefore, this can trigger distrustin the different partners of the agri-tech market [45]. The direction towards implementing IPM inthis system could provide better outcomes to the post-harvest market. However, there is still a lot ofwork to be done to completely tune the system into providing robust disease control. In addition tothe different approaches included in this section, interventions based on the exploitation of the plantand fruit immune system are being developed [2]. They explore the possibility of triggering inducedresistance mechanisms in the fruit, which could constitute an additional element in IPM to reduceultimately the amount of pesticides used in agricultural systems [18].

4. Induced Resistance for Post-Harvest Disease Protection

In the search for more environment-friendly strategies, many studies have investigated whetherthe induction of resistance in the host fruit could serve as an effective approach to combat post-harvestwaste through diseases. In a recent review publication by Romanazzi and colleagues, it was shownthat the number of papers describing induced resistance responses post-harvest have consistentlyincreased through the years, demonstrating the potential of this particular field [2]. In a first study inthe early 1990s, Chalutz et al. (1992) demonstrated that the activation of the induced resistance capacityof fruit can represent a method for disease control [46]. This study reported that exposure of citrus toUV light resulted in induced resistance against green mould fungal disease caused by P. digitatum.

Other methods of defence induction have been reported, including other physical strategies,plant-produced and biological compounds, biocontrol agents and microbe-associated molecularpatterns (MAMPs) (Figure 1). The mechanisms by which these strategies trigger inducedresistance are very diverse; however, they can be characterized in key groups: (1) accumulation ofpathogenesis-related (PR) proteins and hormone-dependent signalling; (2) activation of the antioxidantmachinery—reactive oxygen species (ROS) and enzymes such as catalase (CAT), peroxidase (POD),ascorbate peroxidase (APX), and superoxide dismutase (SOD); (3) and antimicrobial enzymatic activityof fruit–phenolic compounds, lignin and enzymes such as chitinases (CHI), glucanases (GLU) andphenylalanine ammonia-lyase (PAL) (Figure 1).

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Figure 1. Methods and mechanisms of defence induction. Methods include physical strategies, chemicals, biocontrol and microbe-associated molecular patterns (MAMPs). Mechanisms are classified in signalling functions (accumulation of pathogenesis related (PR) proteins and hormone-dependent signalling), antioxidant functions (reactive oxygen species (ROS) and antioxidant enzymes), and antimicrobial functions (phenolics, lignins and antimicrobial enzymes).

4.1. Physical Approach

From that initial paper from Chalutz et al. (1992) other studies have further demonstrated the effect of low-dose UV light in the resistance of fruit to pathogens. They have linked the resistance with the production of antifungal compounds [47] and changes in the activity of defence-related enzymes [48]. In addition to this effective method, other physical approaches have been shown to enhance the resistance capacity of the host. For instance, microarray analysis of heat-exposed peach fruit demonstrated the induction of genes previously involved in resistance such as transcription factors [49]. Moreover, treatment of strawberries with hot air directly triggered the accumulation of PAL, CHI, as well as CAT, APX and SOD, which in turn resulted in the size reduction of lesions caused by B. cinerea [50]. In addition, exposing strawberry fruit to hypobaric conditions has also been shown to trigger induced resistance against B. cinerea and Rhizopus stolonifera, linked to increased CHT, PAL and POD activity [51].

4.2. Chemical Approach

The use of chemicals, including fungicides and plant- and biologically-derived compounds, to induce resistance post-harvest has been studied in depth in different pathosystems. Some of these chemicals are plant hormones such as jasmonic acid (JA) and salicylic acid (SA) that are directly responsible for the induction of defence pathways that result in enhanced protection to different diseases. Whereas JA is mostly associated with induced resistance against necrotrophic pathogens, SA is generally involved in mounting defence mechanisms against biotrophic pathogens, through induced systemic resistance (ISR) and systemic acquired resistance (SAR), respectively [52,53]. Importantly, both hormones display in some conditions an antagonistic effect that helps the plant prioritizing a defence strategy over another [54]. The induced resistance effect of a plant hormone in fruit has been studied in depth. For example, the methylated form of JA, MeJA, was shown to be effective in enhancing resistance in peach fruit against P. expansum, B. cinerea or R. stolonifera through increased levels of pathogenic proteins and antimicrobial compounds [55]. Additionally to the fungicidal direct effect [56], treatments with SA have also been proven effective in inducing resistance in fruit against different fungal pathogens, including P. expansum, P. digitatum, P. italicum and A.

Figure 1. Methods and mechanisms of defence induction. Methods include physical strategies,chemicals, biocontrol and microbe-associated molecular patterns (MAMPs). Mechanisms are classifiedin signalling functions (accumulation of pathogenesis related (PR) proteins and hormone-dependentsignalling), antioxidant functions (reactive oxygen species (ROS) and antioxidant enzymes), andantimicrobial functions (phenolics, lignins and antimicrobial enzymes).

4.1. Physical Approach

From that initial paper from Chalutz et al. (1992) other studies have further demonstrated theeffect of low-dose UV light in the resistance of fruit to pathogens. They have linked the resistancewith the production of antifungal compounds [47] and changes in the activity of defence-relatedenzymes [48]. In addition to this effective method, other physical approaches have been shown toenhance the resistance capacity of the host. For instance, microarray analysis of heat-exposed peachfruit demonstrated the induction of genes previously involved in resistance such as transcriptionfactors [49]. Moreover, treatment of strawberries with hot air directly triggered the accumulation ofPAL, CHI, as well as CAT, APX and SOD, which in turn resulted in the size reduction of lesions causedby B. cinerea [50]. In addition, exposing strawberry fruit to hypobaric conditions has also been shownto trigger induced resistance against B. cinerea and Rhizopus stolonifera, linked to increased CHT, PALand POD activity [51].

4.2. Chemical Approach

The use of chemicals, including fungicides and plant- and biologically-derived compounds,to induce resistance post-harvest has been studied in depth in different pathosystems. Some of thesechemicals are plant hormones such as jasmonic acid (JA) and salicylic acid (SA) that are directlyresponsible for the induction of defence pathways that result in enhanced protection to differentdiseases. Whereas JA is mostly associated with induced resistance against necrotrophic pathogens, SAis generally involved in mounting defence mechanisms against biotrophic pathogens, through inducedsystemic resistance (ISR) and systemic acquired resistance (SAR), respectively [52,53]. Importantly, bothhormones display in some conditions an antagonistic effect that helps the plant prioritizing a defencestrategy over another [54]. The induced resistance effect of a plant hormone in fruit has been studiedin depth. For example, the methylated form of JA, MeJA, was shown to be effective in enhancingresistance in peach fruit against P. expansum, B. cinerea or R. stolonifera through increased levels ofpathogenic proteins and antimicrobial compounds [55]. Additionally to the fungicidal direct effect [56],treatments with SA have also been proven effective in inducing resistance in fruit against differentfungal pathogens, including P. expansum, P. digitatum, P. italicum and A. alternata. Antimicrobial andantioxidant enzymes have been involved in the expression of this induced resistance response in

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many plant species, including citrus fruit, apricots, mangoes and cherries [30,57]. The SA-mimickingagent Benzo (1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH) has also been shown to triggerinduced resistance in melons against Trichothecium roseum and mediated by an increased activityof ROS [58]. Also, it has been shown to reduce infection of T. roseum in cucurbits such as certainvarieties of melon through the activation of the phenylpropanoid pathway [59]. Other plant hormoneshave also been described to trigger induced resistance in fruit at a post-harvest level. Nitric Oxide(NO) is a gaseous compound associated with the production of reactive oxygen species, is implicatedin many different signalling processes in the plant, and has also been shown to play a role in fruitresistance to diseases. For instance, it was reported that external applications of NO could lead to areduction in citrus fruit anthracnose caused by C. gloeosporioides [60]. Its induced resistance activity wastotally linked to changes in hydrogen peroxide (H2O2) levels. Moreover, the accumulation of phenoliccompounds and the induction of enzymes such as PAL, POD, CAT and the ascorbate–glutathionecycle were also described to play a role in the induced resistance response.

Other chemicals have also been described to trigger induced resistance post-harvest. Treatmentswith the chemical volatile trans-2-hexenal triggers induced resistance against B. cinerea in tomatofruit that is mediated by the activation of ethylene responsive genes and PAL [61]. Another set ofchemicals that have been shown to trigger induced resistance at a post-harvest level are β and γ-aminobutyric acid, known as BABA and GABA, respectively [62,63]. BABA is a well-studied non-proteinamino acid that primes defence mechanisms through multiple signalling pathways in a wide range ofplant species [63]. Recently, its biosynthesis has been demonstrated in various plants, thus promotingBABA to the rank of natural phytohormones [64]. Its effect is better understood in vegetative tissuebut it has also been shown that BABA can result in induced resistance post-harvest against differentdiseases [63]. BABA has been reported to trigger IR through priming against more than 50 bioticand abiotic threats, including fungi, bacteria, herbivory, viruses and drought [63,65]. Importantly,BABA-IR has been proven to be long-lasting in Arabidopsis thaliana [11] and tomato [10] and its primingeffect was even transmitted to the following generations [13], most likely through changes in theepigenetic machinery of plants. Very recently, we showed that BABA-IR, after application of thechemical to tomato seedlings, was maintained to the fruiting stage providing protection againstB. cinerea post-harvest [17]. This induced resistance was associated to accumulation of the planthormone abscisic acid (ABA) in the fruit and highlights a complex role of this plant hormone inBABA-IR. This long-lasting induced resistance was observed in fruit after the treatment of seedlings;however, fruit failed to maintain the resistance phenotype when the treatment had been done oncefruit had been produced. GABA is also known for its induced resistance effect, however, in comparisonto BABA, the spectrum of action of this chemical is limited [66–68]. Nevertheless, GABA treatmentsseem effective against rot caused by A. alternata in tomato fruit. Whereas no direct antifungal effectwas observed, GABA was demonstrated to trigger resistance through induction of the antioxidantmachinery of the fruit, through the activation of CAT, SOD and POD enzymes.

4.3. Biocontrol

Yeast cultures are the most used method of biocontrol of post-harvest diseases against fungalpathogens. Apart from the direct effect in the production of enzymes that degrade pathogenstructures [69] and competition for space, different strains have been linked to the activation ofresistance mechanisms in fruit. For example, strains such as Pichia membranefaciens resulted in theup or down regulation of 25 proteins, which include antioxidants and PR proteins in peach fruit [70].Similarly, strains of Aureobasidium pullulans, and Cryptococcus laurentii, induce resistance in cherrytomatoes and peach, respectively, through the activation of host antioxidants metabolism. In addition,induced resistance activity triggered by A. pullulans has been linked to the accumulation of GLU, CHIand PAL enzymes [71]. In a lesser extent, other methods of biocontrol based in the use of bacterialstrains have been demonstrated to play a role in the activation of induced resistance mechanismspost-harvest. For example, the bacteria Bacillus cereus was proven effective to control anthracnose

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disease caused by Colletotrichum acutatum in loquat fruit through induced production of phenoliccompounds and H2O2 [72].

4.4. Microbe-Associated Molecular Patterns

In addition to microbiological control measures, it has also been shown that the use of microbe-derivedcompounds, known as microbe/pathogen-associated molecular patterns (MAMP/PAMPs) can triggerinduced resistance responses that ultimately result in protection against post-harvest diseases. This isthe case of harpin, a bacterial elicitor that triggers hypersensitive response. Harpin has been shownto induce resistance against A. alternata and Fusarium spp in melons [73] and black spot causedby Guignardia citricarpa in citrus fruit [74]. Treatments with harpin trigger the activation of PAL,4-Coumarate:CoA ligase and GLU and the accumulation of phenolic compounds and lignin [73].Moreover, chitin and other derivatives such as chitosan, are also highly integrated within IPM forthe protection of post-harvest fungal diseases. Chitin and related elicitors are known to result in adirect effect on the pathogen survival due to their capacity to stop spore germination and/or germtube elongation [75]. However, chitin and its derivatives are also responsible for inducing resistancethrough different mechanisms. For example, treatments with the most common derivative chitosantriggered the accumulation of PR proteins, antimicrobial proteins such as GLU and CHI, activationof the antioxidant machinery in fruit through the production of POD, and accumulation of phenoliccompounds [75]. The activation of these defence mechanisms has been linked with the inducedresistance against many different microbes including Monilinia fructicola, B. cinerea and P. italicum inmany different plant species [76–78].

5. Impacts of Induced Resistance

Induced resistance, therefore, provides many benefits, but further research is necessary to fullyintegrate its use with other effective control methods within IPM. Importantly, an induction ofresistance responses can alter other plant processes. In vegetative tissue, this impact is normallyrepresented by trade-offs in plant growth and development [79]. This is driven by a change inthe allocation of energy resources in the plants: when there is an activation of induced resistancemechanisms, plants prevent the allocation of resources to growth as they prioritize the use of energyfor their survival against a threat. Other methods of induced resistance also impact plant growthdue to other factors. For instance, treatments of high concentrations of BABA in Arabidopsis, as aresult of the blocking of the chemical receptor protein (an aspartyl t-RNA synthetase known as IBI1)and the accumulation of the canonical substrate, uncharged tRNA, result in growth reduction [80].Many groups have investigated the impact of the activation of induced resistance in fruit developmentand quality. Intuitively, it could be expected that activation of induced resistance would automaticallyalter fruit growth and quality negatively. However, as seen in this section, many methods of inducingresistance have been correlated with the activation of the antioxidant machinery of the fruit, whichcould potentially lead to enhanced benefits for human consumption.

Fatemi et al., 2013 for instance, demonstrated that kiwi fruit that harboured increased resistance togrey mould after application of the plant hormone SA, displayed better values in various post-harvestquality factors, including titratable acidity (TA), levels of antioxidants and ascorbic acid (AA) [81].Similarly, exogenous NO application has been shown to increase AA, TA, and total soluble solids(TSS) content in citrus fruit [60], and treatment with MeJA increases AA content in tomato fruit [82].In contrast, the application of SA and yeast biocontrol to induce resistance against grey mould did notimpact quality properties in peach fruit [83]. In the same lines, treatments of bananas with SA, theSA-mimicking agent BION and K2HPO did not result in changes in any of the quality characteristicsmonitored, including fruit weight, firmness, TSS and TA [84]. On the contrary, treatments withtrans-2-hexenal were shown to trigger undesirable changes in the flavour and odour of peach, apricotand nectarine fruit [85]. In addition, we have recently demonstrated that treatments with BABA dohave consequences on fruit development and quality by affecting other structural parameters such as

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fruit size and colour [17]. Tomatoes that came from plants treated with BABA, at the seedling stageand when the fruit had been produced (still green), showed delayed fruit production and ripening.In addition, traces of BABA were found in these tomatoes, which warns of potential risks in commercialapplications of this approach [17]. Whether BABA affects chemical fruit content, TA or TSS remains tobe elucidated. Nevertheless, it is important to keep these parameters in mind when exploiting inducedresistance in fruit, as noticeable changes can hinder the commercialization of the products.

6. Towards the Future: Exploiting Priming

6.1. Priming for Fruit Resistance

As a more adapted strategy to the expression of defence responses in the fruit via inducedresistance, priming of defence mechanisms could provide a solution towards potentially undesirablecosts in fruit quality. Primed fruit or plants would not directly activate defence mechanisms unless achallenge is encountered. The costs and benefits of priming with or without second challenge havebeen extensively documented [16], and studies clearly conclude that upon infection, the benefits thatplants obtain from activating primed defence mechanisms outweigh the costs.

Different studies have investigated the possibility that priming in fruit marks induced resistancein fruit post-harvest. For instance, treatments with the chemical GABA in pear fruit result in aninduced resistance against P. expansum that is based on priming of accumulation of GLU an CHIproteins [66]. Similar priming responses were observed in the induced resistance response triggeredby Candida saitoana against B. cinerea in apple fruit [86]. Moreover, Bacillus cereus-mediated inducedresistance against C. acutatum in loquat fruit is based in priming of expression of defence-related genes(e.g., NPR1, PAL and EIN3) [72]. Thus, induced resistance in fruit can be marked by priming of defence.

6.2. Key Aspects for Exploiting Priming in Fruit

There are different aspects that make priming of defence an appealing phenomenon to study(Figure 2).

Plants 2018, 7, x FOR PEER REVIEW 9 of 16

production and ripening. In addition, traces of BABA were found in these tomatoes, which warns of potential risks in commercial applications of this approach [17]. Whether BABA affects chemical fruit content, TA or TSS remains to be elucidated. Nevertheless, it is important to keep these parameters in mind when exploiting induced resistance in fruit, as noticeable changes can hinder the commercialization of the products.

6. Towards the Future: Exploiting Priming

6.1. Priming for Fruit Resistance

As a more adapted strategy to the expression of defence responses in the fruit via induced resistance, priming of defence mechanisms could provide a solution towards potentially undesirable costs in fruit quality. Primed fruit or plants would not directly activate defence mechanisms unless a challenge is encountered. The costs and benefits of priming with or without second challenge have been extensively documented [16], and studies clearly conclude that upon infection, the benefits that plants obtain from activating primed defence mechanisms outweigh the costs.

Different studies have investigated the possibility that priming in fruit marks induced resistance in fruit post-harvest. For instance, treatments with the chemical GABA in pear fruit result in an induced resistance against P. expansum that is based on priming of accumulation of GLU an CHI proteins [66]. Similar priming responses were observed in the induced resistance response triggered by Candida saitoana against B. cinerea in apple fruit [86]. Moreover, Bacillus cereus-mediated induced resistance against C. acutatum in loquat fruit is based in priming of expression of defence-related genes (e.g., NPR1, PAL and EIN3) [72]. Thus, induced resistance in fruit can be marked by priming of defence.

6.2. Key Aspects for Exploiting Priming in Fruit

There are different aspects that make priming of defence an appealing phenomenon to study (Figure 2).

Figure 2. Priming strategies for long-lasting disease resistance in fruit. The described methods of induced resistance are effective from different stages of plant and fruit development. Their expression is based on different mechanisms that can impact the defence capacity of the plant in a short or long-lasting manner. The expression of priming has different advantages and disadvantages depending on when stimuli are applied.

Figure 2. Priming strategies for long-lasting disease resistance in fruit. The described methods ofinduced resistance are effective from different stages of plant and fruit development. Their expression isbased on different mechanisms that can impact the defence capacity of the plant in a short or long-lastingmanner. The expression of priming has different advantages and disadvantages depending on whenstimuli are applied.

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Priming is known to result in broad-spectrum resistance due to the target of many differentmechanisms. In different systems, priming agents such as BABA and R-β-homoserine (RBH) have beendescribed to trigger induced resistance through priming against diseases of very different natures [87].In Arabidopsis, RBH was effective against the biotrophic pathogen Hyaloperonospora arabidopsidis andthe necrotrophic pathogen Plectosphaerella cucumerina thanks to the priming of many different defencesignalling pathways. In addition, it is easy to identify from the information summarised in Figure 1 thatthere are induced resistance agents that can activate many different resistance processes. For instance,yeast biocontrol by A. pullulans has been shown to trigger GLU, CHI and PAL which in turn results inresistance to pathogens with different lifestyles, such as B. cinerea [88] and P. expansum [89]. It is likelythen, that the priming of those induced resistance mechanisms is behind the protection against all thosemany different biotic stresses. In addition, priming has also been described to represent a mechanismof enhanced tolerance to drought and temperature stresses [90]. Fruit, as happens with plants duringtheir growing period, can face abiotic stresses. Priming responses have also been linked to enhancedtolerance of peach fruit against chilling injury [91]. Moreover, it was demonstrated that treatmentsof tomato fruit with SA, for instance, also provides tolerance to cold damage during storage [92].Therefore, it is plausible that the priming of defence in fruit does also result in protection againstabiotic damage triggered by temperature, moisture or mechanical damage due to lack of fruit firmness.

It is also important, however, to take into consideration that there are agents that trigger a specificinduced resistance response that is effective against a particular subset of stresses. For instance,trans-2-hexenal results in the activation of ethylene responsive genes and PAL, however, does notinduce the accumulation of the PR proteins (e.g., PR-1a and PR-5) [61]. This agent, which leads tothe protection against the necrotrophic pathogen B. cinerea, could be hindered in the activation of acrucial defence pathway against other pathogens, thus compromising the resistance capacity of thefruit. Moreover, hormone-dependent signalling pathways display antagonistic responses. The bestcharacterised crosstalk of hormone pathways is between SA and JA: the activation of SA-dependentsignalling results in the downregulation of the pathways under the control of JA, and vice versa [54].Therefore, it is plausible that post-harvest induced resistance by agents such as SA, BION or MeJAcould result in the downregulation of their counterparts and, therefore, produce fruit that is moresusceptible to other specific stresses. Further research is crucial to determine the different responsesassociated with the use of the priming of defence.

Priming has also been shown to be a long-lasting response [10,11] and even to be transmitted tosubsequent generations [12–14]. Therefore, priming is a unique form of plant memory. Long-lastingstudies support the idea that, similarly to what happens with other control means, an early stimulationduring the pre-harvest stage could plausibly provide long-lasting priming that could reach thefruiting stage. This approach would not only benefit from the advantages of early interventionwhen diseases have not yet fully established themselves, but also could prevent associated costsof induced resistance (Figure 2). Early treatments at a preharvest level with SA and BABA havebeen shown to reduce disease incidence of P. digitatum and B. cinerea in orange and tomato fruit,respectively [17,93]. In the case of BABA, the long-lasting induced resistance response correlated withthe differential accumulation of metabolites putatively identified as lipids, alkaloids, terpenoids andthe plant hormone ABA [17]. This subset of metabolites was speculated to act as a priming fingerprintthat marks the better expression of defence mechanisms in fruit. Importantly, however, inducedresistance was not observed in fruit when the treatment of plants with BABA was performed afterthe fruit had been produced, thereby pointing to the lack of chemical relocation to the fruit as theywere no longer sinks. However, further research is needed to unravel whether long-lasting SA- andBABA-IR are based on priming of defence mechanisms. Other biological agents are also established atearly stages of plant growth, for instance, arbuscular mycorrhizal fungi (AMF). These beneficial fungihave been linked to the activation of priming responses in different crop species, including tomatoand wheat [94,95]. However, it is not known whether AMF-induced resistance can reach the fruitingstage and can result in post-harvest protection. Therefore, further research is necessary to address

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this question, which could foster new strategies based on the use of beneficial microorganisms forlong-lasting induced resistance in the fruit.

Interestingly, the long-lasting nature of priming, more commonly understood as a plant memory,has been linked to the activity of epigenetic mechanisms that could fine-tune the expression ofdefence responses. These studies have been mainly based in Arabidopsis, however, there isevidence that the expression of priming in other crops such as potato and common bean is alsolinked to epigenetic modifications [96,97]. For instance, long-lasting and transgenerational activityof priming of SA-dependent gene expression relies in changes in chromatin modifications andDNA methylation [11,12]. This brings up the question: can epigenetic changes also be mediatingthe expression of priming in fruit? It has been previously described that processes such as fruitdevelopment and ripening are under the control of chromatin modifications and changes in DNAmethylation [98]. Similarly, they have been demonstrated to play certain role in post-harvestprocesses [99,100]. Considering that fruit are maternal tissue, and having in mind that some pesticideswith use pre-harvest can trigger induced resistance and have been linked with epigenetic changes [101],it is very plausible that epigenetic mechanisms play certain role in priming processes in fruit. Actually,changes in the expression of chromatin modification genes have been shown in sweet orange fruitupon infection with P. digitatum [102]. The potential of this field is undeniable and it is, therefore,necessary to explore these pathways for disease control. Epigenetic mechanisms could secure an earlyimprinting of the priming phase towards a faster and stronger disease response in fruit that couldcontribute to the protection of fruit to post-harvest diseases.

7. Concluding Remarks

Overall, induced resistance and priming have emerged as efficient strategies that can contributeto the protection against post-harvest diseases, thereby providing effective alternatives to pesticides forthe control of such diseases. Priming-based induced resistance has several benefits: (i) it does not triggera direct activation of defences therefore does not incur in major costs in growth and development;(ii) it provides broad-spectrum resistance; and (iii) it is long-lasting and can reach the fruiting stage.Nevertheless, induced resistance and priming have also been linked to undesirable effects in fruitquality and other untargeted effects, including susceptibility phenotypes as result of crosstalks in theactivation of defence mechanisms. The comprehensive understanding of responses and the adaptationof induced resistance and priming into IPM could provide solutions with a real effect in the protectionof fruit post-harvest. With respect to this, the use of computational tools in agricultural research, suchas machine learning, would provide a better picture of the multi-layered regulations that occur uponinduced resistance [103]. In addition, for instance, the combination of different induced resistanceagents has been described in other settings with successful results [79]. Importantly, broad-spectrumpriming agents such as BABA do not impact the establishment of beneficial microorganisms such asarbuscular mycorrhizal fungi in tomatoes [10]. Thus, IPM and the provision of plants with differenttools that prime their immune system could lead to a successful strategy towards the protection offruit post-harvest and overall food security for the ever-growing world population.

Author Contributions: E.L. and P.P. equally contributed to the conception and writing of the manuscript. P.P.,A.L. and E.L. provided intellectual input and critically revised the manuscript.

Funding: This work was funded by the BBSRC Future Leader Fellowship BB/P00556X/1 to E.L., by BordeauxUniversity and INRA, Bordeaux Metabolome Facility and MetaboHUB (ANR-11-INBS-0010 project) to P.P., and bythe H2020-MSCA-IF-2016-EPILIPIN-746136 to A.L.

Acknowledgments: The authors thank Julio Aparicio Gallego for providing expertise regarding pesticide usepost-harvest. The authors also thank Samuel W Wilkinson for his input during the development of this lineof research.

Conflicts of Interest: The authors declare no conflict of interest.

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